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Jun 20, 2007 - Abstract The aim of the present study was to assess the heat tolerance of animals of two Portuguese (Alentejana and Mertolenga) and two ...

Int J Biometeorol (2008) 52:199–208 DOI 10.1007/s00484-007-0111-x

ORIGINAL PAPER

Effect of thermal stress on physiological parameters, feed intake and plasma thyroid hormones concentration in Alentejana, Mertolenga, Frisian and Limousine cattle breeds Alfredo M. F. Pereira & Flávio Baccari Jr. & Evaldo A. L. Titto & J. A. Afonso Almeida

Received: 16 January 2007 / Revised: 8 May 2007 / Accepted: 22 May 2007 / Published online: 20 June 2007 # ISB 2007

Abstract The aim of the present study was to assess the heat tolerance of animals of two Portuguese (Alentejana and Mertolenga) and two exotic (Frisian and Limousine) cattle breeds, through the monitoring of physiological acclimatization reactions in different thermal situations characterized by alternate periods of thermoneutrality and heat stress simulated in climatic chambers. In the experiment, six heifers of the Alentejana, Frisian and Mertolenga breeds and four heifers of the Limousine breed were used. The increase in chamber temperatures had different consequences on the animals of each breed. When submitted to heat stress, the Frisian animals developed high thermal polypnea (more than 105 breath movements per minute), which did not prevent an increase in the rectal temperature (from 38.7°C to 40.0°C). However, only a slight depression in food intake and in blood thyroid hormone concentrations was observed under thermal stressful conditions. Under the thermal stressful conditions, Limousine animals decreased

A. M. F. Pereira (*) : J. A. A. Almeida ICAM, Instituto de Ciências Agrárias Mediterrânicas, Universidade de Évora, Apartado 94, 7000-554 Évora, Portugal e-mail: [email protected] J. A. A. Almeida e-mail: [email protected] F. Baccari Jr. UNESP, Botucatu, Brazil e-mail: [email protected] E. A. L. Titto FZEA-USP, Pirassununga, Brazil e-mail: [email protected]

food intake by 11.4% and blood triiodothyronine (T3) hormone concentration decreased to 76% of the level observed in thermoneutral conditions. Alentejana animals had similar reactions. The Mertolenga cattle exhibited the highest capacity for maintaining homeothermy: under heat stressful conditions, the mean thermal polypnea increased twofold, but mean rectal temperature did not increase. Mean food intake decreased by only 2% and mean T3 blood concentration was lowered to 85,6% of the concentration observed under thermoneutral conditions. These results lead to the conclusion that the Frisian animals had more difficulty in tolerating high temperatures, the Limousine and Alentejana ones had an intermediate difficulty, and the Mertolenga animals were by far the most heat tolerant. Keywords Cattle . Mediterranean . Heat stress . Thyroid hormones . Acclimatization

Introduction In order to maximize cattle production allowed by their genetic potential, allowing better system organisations, it is important to improve the knowledge about the physiology and behavior of the animals from different breeds. The hot and dry summers of the Mediterranean climate impose severe thermal stress and food shortage on the grazing animals, potentially compromising the productivity of the less adapted breeds. Alentejana and Mertolenga are the most representative native Portuguese cattle breeds (Bos taurus). They are raised mainly in rangeland conditions and are also utilized for industrial crosses with exotic breeds, mainly Charolês and Limousine.

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It is important to understand the effects of heat stressful summer conditions on the homeostasis of the most utilized cattle breeds in Mediterranean rangeland areas, in order to maximize the intensification levels of the production systems and to improve animal welfare and their production efficiency. However, there is no previous scientific information about the thermal tolerance of these breeds. Different breeds exhibit different reactions to unfavorable environmental thermal conditions. At high temperatures, Bos indicus animals perform better than Bos taurus ones, due to their higher tolerance to heat stress. Their lower metabolic rate, thinner fur and their more efficient heat loss mechanisms are the most important traits explaining the better heat tolerance and productivity of zebu type cattle under hot conditions (Colditz and Kellaway 1972; Frisch and Vercoe 1984; Spiers et al. 1994). However, within the less heat tolerant European cattle breeds (Bos taurus), there are anatomic and physiological differences which could explain different levels of thermal tolerance (Amakiri and Funsho 1979; Berbigier 1983; Kamal et al. 1992; Titto et al. 1998). The main consequence of the heat stress on animal productivity is related to a decrease of food intake. The lower food intake together with a decrease in blood circulating thyroid hormone levels determine lower metabolic and thermogenic rates, which explain the decrease of animal productivity during acclimatization to chronic stressful heat conditions (Bianca 1965; Alnaimy et al. 1992; Zia-Ur-Rehman et al. 1982). The relationships between thyroid hormone concentrations and food intake are very complex. Several research studies have shown that the lower concentrations of thyroid hormones are not a primary consequence of a lower food intake, resulting mainly from complex neuro-endocrine processes related to the sequential interactions among thermosensors, hypothalamus, adenohypophysis and thyroid (Bianca 1965; Zia-Ur-Rehman et al. 1982; Alnaimy et al. 1992; Silanikove 2000). Even so, the decrease in the blood triiodothyronine and thyroxine concentrations reinforce the tendency for a depressed food intake (Riis 1983). An increase in body heat inhibits the TSH Releasing Hormone (TRH) secretion by the hypothalamus, consequently decreasing the Thyroid Stimulating Hormone (TSH) secretion from adenohypophysis, leading to a lower thyroid activity (Berman 1968; Muller et al. 1994). However, in some studies, normal concentrations of TSH were observed with simultaneous low concentrations of triiodothyronine and thyroxine, suggesting a direct effect of body heat on the thyroid metabolism, resulting, probably, from the stimulation of the thyroid sympathetic innervations which determine an inhibitory or refractory action related to the TSH (Magdub et al. 1982; Silva 2000). Therefore, thyroid hormones are of utmost importance in

Int J Biometeorol (2008) 52:199–208

the heat adaptation process, allowing the adjustment of the metabolic rates in favor of the body heat balance. The objective of this study was to compare the physiological reactions of animals of the Alentejana, Mertolenga, Frisian and Limousine breeds to thermically stressful conditions and to evaluate the heat stress effects on food and water intakes and on the thyroid hormones in the animals of those different breeds.

Material and methods The experiment was carried out in two climatic chambers each of 45 m2, enabling the simultaneously housing of a total of 12 animals (6 in each climatic chamber). Air temperature control was achieved by heating or chilling the air flow entering the chamber from six openings, placed at 2.8 m height, along its longitudinal axis. The air was heated using a gas boiler, and was cooled by passing through chilled serpentines. Humidity control was carried out using humidifiers and recorded by hygrothermographs. The environmental climatic parameters inside the chambers were set through a main control centre, placed outside the chambers. The maintenance of the selected environmental parameters was automatically controlled by temperature/ humidity sensors placed in the entrance and exit of the climatic chambers. The temperature and humidity control system responded very rapidly and precisely to the elicited thermal changes. The system has a low thermal inertia. After changing the thermal parameters of the climatic chambers, the new temperature and humidity were reached approximately within 50 min with an accuracy ±1°C. Twenty-two heifers, 6 Alentejana, 6 Mertolenga (Bos Taurus portuguese native cattle breeds), 4 Limousine and 6 Frisian, were used. The initial average body weights were 340.1±19.4 kg; 235.0±28.8 kg; 389.7±38.9 kg and 289.1± 16.9 kg, respectively. The Alentejana, Mertolenga, Limousine and Frisian animals ended the 13th day experimental period weighing 346.7±16.4 kg; 241.2±24.8 kg; 394.8±37.7 kg and 297.0±14.2 kg, respectively. Two months before the experiment the animals were handled, head haltered and trained, in order to decrease reactivity and obtain a better adjustment to the new management and environment. Due to the limited space of the two chambers, the experiment was conducted during two different trials with 12 and 10 animals, respectively, both with the four breeds present and with at least 2 animals per breed. The heifers were kept in individual stalls (3.0×1.1 m) and restrained by a head halter. Each period lasted 18 days, 5 for adaptation and 13 for data collection. The adaptation period (in thermoneutral conditions) was for the adjustment or habituation of the

Int J Biometeorol (2008) 52:199–208

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animals to the physical environment and to the various routines they would face during the test. In order to evaluate the reactions to thermically stressful conditions, the experiment was designed with three different periods. During periods 1 and 3, environmental conditions were set to be thermoneutral while period 2 was heat stressful. The internal climatic chamber environments were set as follows: (1) a 3-day period (period 1, P1) with air temperature (Ta) and relative humidity (rH) kept at 16.5°C and 45% (thermoneutral, TN); (2) a 6-day period (period 2, P2) with Ta and rH kept at 36.0°C and 45% from 0800 to 1630 hours and 26.5°C and 60% from 1630 to 0800 hours, both considered to be thermically stressful (TS); and (3) a 4-day period (period 3, P3) which Ta and RH again kept at 16.5°C and 45% (thermoneutral, TN). Diet was composed of 85% maize silage and 15% sunflower meal (Table 1). Food and water were available ad libitum, with fresh food provided twice per day at 0830 and 1630 hours. Ingestion (I) was calculated based on the differences between the food offered and the food refused. Water was provided using automatic waterers and measured through a dispenser (accuracy ±0.01 l). Daily food (f) and water (wt) intakes were expressed on a metabolic weight base (Body Weight 0,75). Respiratory frequencies (RF) were measured by observing costal movements during 30 s and rectal temperatures (RT) were measured using a digital thermometer (Digitron, with an 8-cm flexible probe). RF and RT measurements were carried out every day at 0800, 1230, 1530 and 1830 hours. Blood samples (7.5 ml each) were collected at 1400 hours, from the jugular vein, into Sarstedt Monovete Serum Gel tubes (ref. 01.1602) on days 3 (P1, TN), 6 (P2a, TS), 9 (P2b, TS) and 13 (P3, TN). An aliquot of each sample was utilized for Hematocrit determination, and blood serum was obtained by immediate centrifugation (10 min, 4°C, 1 500 g) in a J-6B centrifuge (Beckman, Buckinghamshire, UK) and frozen (−80°C) in a UF460 freezer (Heto, Brondby, Denmark) until analysis. Two blood samples were collected during the TS period in order to improve the understanding of the endocrine readjustment to thermal stress. Hematocrit was measured in blood aliquots by a Sysmex F8000 Analyser. Blood cortisol, triiodothyronine and thyroxine concentrations were determined by radioimmunoassay using an Auto

Table 1 Dietary composition (%): dry matter (DM), crude protein (CP), crude fibre (CF), fat and ash

Maize silage (MS) Sunflower meal (SM) Diet (85 MS + 15 SM)

DM

CP

CF

Fat

Ash

27.0 96.0 37.8

8.1 31.8 11.6

23.8 21.8 23.5

4.2 1.5 3.8

5.3 6.1 5.4

Analyser Access Immunoassay System based and commercial available kits. Different statistical models were used to analyse different variables. Due to the limited space of the chambers, two different trials were conducted sequentially. In order to detect eventual differences between trials, a previous statistical analysis was made comparing the results obtained from the two trials (12 animals in the first and 10 animals in the second trial). As no significant differences were observed (P=0,923) between the results obtained for each variable, data were pooled for statistical analysis. RF and RT data were analyzed according to a general linear model procedure with 3 fixed factors and 1 nested factor: Yijklm ¼ m þ Bi þ Bð AÞið jÞ þ Pk þ Hl þ B:Pik þ B:Hil þ P:Hkl þ B:P:Hikl þ "ijklm where Yijklm are the observed values of rectal temperature or respiratory rate, μ the observed mean value, Bi fixed effect of breed; B(A)i(j) nested effect of animal within breed, Pk fixed effect of temperatures period, Hl fixed effect of the hour, B.Pik interaction breed–period, B.Hil interaction breed–hour, P.Hkl interaction period–hour, R.F.Hikl triple interaction breed–period–hour, and ɛijklm random error or residual effect. Food and water intakes were analyzed according to a general linear model procedure with 2 fixed factors and 1 nested factor: Yijkl ¼ m þ Bi þ Bð AÞið jÞ þ Pk þ B:Pik þ "ijkl where Yijklm are the observed values for feed and water intakes, μ observed mean value, Bi fixed effect of breed, R (A)i(j) nested effect of animal within breed, Pk fixed effect of temperatures period, B.Pik interaction breed–period, and ɛijkl random error or residual effect. Blood parameters were analyzed according to a general linear model procedure with 2 fixed factors and 1 nested factor: Yijkl ¼ m þ Bi þ Bð AÞið jÞ þ Dk þ B:Dik þ "ijkl where Yijklm are the observed values for hematocrit or cortisol or thyroid hormones, μ observed mean value, Bi fixed effect of breed, R(A)i(j) nested effect of animal within breed, Dk fixed effect of date of blood samples, B.D.ik interaction breed–date, and ɛijkl random error or residual effect. Significantly different means were submitted to post-hoc comparisons of means (Tukey-Hsu test) and regarded as significantly different when P

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